A dietary perspective of cat-human interactions in two medieval harbors in Iran and Oman revealed through stable isotope analysis

Cats are hypercarnivorous, opportunistic animals that have adjusted to anthropogenic environments since the Neolithic period. Through humans, either by direct feeding and/or scavenging on food scraps, the diet of cats has been enriched with animals that they cannot kill themselves (e.g., large mammals, fish). Here, we conducted carbon and nitrogen stable isotope ratio analysis to reconstruct the diet of medieval cats and investigate cat-human interactions in two medieval harbor sites (Qalhât, Oman and Siraf, Iran). The analysis included 28 cat individuals and 100 associated marine and terrestrial faunal samples pertaining to > 30 taxa. The isotopic results indicate a high marine protein-based diet for the cats from Qalhât and a mixed marine-terrestrial (C4) diet for the cats from Siraf. Cats at these sites most likely scavenged on both human food scraps and refuse related to fishing activities, with differences in the two sites most likely associated with the availability of marine resources and/or the living conditions of the cats. By shedding light on the dietary habits of cats from two medieval harbors in the Arabian Gulf and Gulf of Oman, this study illustrates the potential of stable isotope analysis in reconstructing human-cat interactions in the past.


Materials and methods
The cat remains and associated fauna analyzed in this study are from two medieval harbor towns, Siraf in Iran and Qalhât in Oman (Fig. 1). The faunal spectra of the two sites can be adequately compared since in both cases, the zooarchaeological analyses were carried out on large animal refuse accumulations that were sampled in the same way (i.e., by hand-collection). Table 1 presents the relative importance of the major food animals at Qalhât and Siraf, based on the zooarchaeological evidence.
Qalhât, located near the easternmost tip of the Arabian Peninsula, was a large town occupied between the eleventh and sixteenth centuries CE. It was one of the major ports of the region between the thirteenth and fifteenth centuries, when it dominated the maritime trade in the western Indian Ocean and the Arabian Gulf. It was struck by an earthquake at the end of the fifteenth century, then plundered by the Portuguese in 1508 and finally completely abandoned in the second half of the sixteenth century 42 . Fieldwork since 2008 has revealed the layout of medieval Qalhât and has located the town's major buildings. The cat remains included in the present study belong to 12 domestic cats (of which 3 were non-adult, weaned individuals, cf. Supplementary Table 1) and Table 1. Proportions (%) at Siraf and Qalhât of (1) the major animal groups, (2) the main domestic species, and (3) the major ecological fish groups, based on identifications provided in von den Driesch and Dockner 36 for Siraf and in Marrast 37 and Monchot 46 for Qalhât. The number of specimens on which the percentages were calculated are given in brackets. For Siraf, the numbers correspond to specimens that date to the first millennium CE, which is the period from which almost all samples for isotopic analysis originate. www.nature.com/scientificreports/ The carbon and nitrogen stable isotope ratios of the samples were determined using a Thermo Flash HT/ EA elemental analyzer linked to a Thermo Delta V Advantage isotope ratio mass spectrometer (IRMS) via a ConfloIV interface (Thermo Scientific) at the Department of Earth and Environmental Sciences of KU Leuven (Belgium). Data calibrations were done using one international (IAEA-600) and two in-house standards (Leucine and muscle tissue of Pacific Tuna) that were prior calibrated against certified standards. The international and in-house standards were measured at regular intervals throughout each analytical run, and their standard deviations defined the analytical error to be better than 0.11‰ for δ 13 C and 0.08‰ for δ 15 N. The isotopic results are presented as the ratio of the heavier to the lighter isotope ( 13 C/ 12 C, 15 N/ 14 N) and are reported relatively to internationally defined standards (VPDB, AIR) as δ values in units per mil (‰).
For estimating the relative contribution of potential food sources to the diet of the cats, we used the Bayesian mixing model FRUITS (Food Reconstruction Using Isotopic Transferred Signals; version 3.0) 54 . The input parameters used for the mixing model are reported in Supplementary Table S5. Wilcoxon signed rank test was performed using the software R (v. 4.1.3.) 55,56 to statistically compare the isotope values of the cats from the two sites. A parametric test was conducted as the size of group samples was small (n < 20) 57 .

Results
Collagen preservation. All 12 cat samples from Qalhât and 10 out of 35 cats from Siraf yielded good quality collagen (i.e., > 13% for %C, > 4.8% for %N, 2.9-3.6 for C:N and ≥ 1% for collagen yield [58][59][60]  Isotopic results from Qalhât. The cats from Qalhât have a mean δ 13 C value of − 11.8‰ (± 0.9‰) and a mean δ 15 N value of 17.1‰ (± 0.7‰). These isotopic values are almost one trophic level above the values of the fish from this site 61,62 , indicating that cats had a diet highly dependent on marine protein. This is further supported by the results of the mixing model (Supplementary Table S6), which suggest that 41 ± 21% of the protein consumed by cats was marine. The fish that yielded acceptable isotopic results have a mean ± SD δ 13 C value of − 11.4 ± 1.1‰ and a mean ± SD δ 15 N value of 14.4 ± 1.2‰ (cf. Supplementary Table 3). Two marine mammals (finless porpoise and small delphinid) have δ 13 C values of − 11.7‰ and − 11.9‰ and δ 15 N values of 15.0‰ and 15.6‰, respectively, reflecting the small fish, crustaceans, cephalopods and/or other mollusks that these two taxa consume. One rat (QALrat01) and one dog (QALdog01) have values that are similar to the values of the cats (i.e., δ 13 C: − 13.6‰ and − 11.4‰, respectively, and δ 15 N: 17.5‰), indicating a significant contribution of marine protein in their diet as well. The remaining four rats have isotope values (δ 13 C mean ± SD: − 18.6 ± 1.3‰ and δ 15 N mean ± SD: 10.6 ± 1.7‰) that reveal different amounts of C 3 , C 4 and marine protein in their diet, while the second dog (QALdog02) has one of the lowest δ 15 N values reported in this study (6.3‰), which could indicate a diet based primarily on C 3 and C 4 plants (δ 13 C: − 15.1‰) 20,63-65 .
With a mean ± SD δ 13 C value of − 15.0 ± 1.1‰ and a mean ± SD δ 15 N value of 16.2 ± 1.5‰, the isotope values of the eight chickens reveal differential amounts of marine protein in their diet. Two wild bird species have δ 13 C (Caspian gull: − 18.9‰ and − 22.1‰ and lappet-faced vulture: − 13.2‰) and δ 15 N (Caspian gull: 14.9‰ and 13.2‰ and lappet-faced vulture: 12.5‰) values that reflect their scavenging nature and the consumption of both terrestrial and marine protein. One lesser white-fronted goose has a δ 13 C value of − 18.7‰ and a δ 15 N value of 15.3‰, which perhaps reflect the consumption of coastal plants (including halophytes 66 ) that were affected by sea-sprays and soil salinity 67,68 , while one cormorant with a δ 13 C value of − 18.3‰ and a δ 15 N value of 12.2‰ likely fed on brackish or a mix of freshwater fish and amphibians as well as marine fish. The latter species may have foraged in Khors (i.e., the typical estuarine habitats found along the Arabian Peninsula's coast) 69,70 . From the wild terrestrial mammals, two gazelle specimens with similar δ 15 N values (7.1‰ and 7.9‰) and a 6.8‰ difference in δ 13 C values (− 19.4‰ and − 12.6‰) reflect the consumption of plants that follow different photosynthetic pathways (i.e., C 3 and C 4 , respectively), while one red fox has a δ 13 C value of − 13.8‰ and a δ 15 N value of 10.1‰, which indicate the consumption of small, wild mammals that were highly dependent on C 4 plants. From the domestic mammals, sheep and goats have similar isotope values that range between − 10.7‰ and − 16.3‰ for carbon and between 5.8‰ and 10.7‰ for nitrogen, reflecting mainly the consumption of C 4 plants, partially at coastal sites 71 . Apart from a high variety of wild C 4 plants in the area 66 , archaeobotanical evidence from the region reveals the presence of cultivated C 4 plants, such as millet 72,73 and sorghum 74 , while historical sources attest that cultivated plants were intended for both human and animal consumption 75 . One sheep has a δ 13 C value of − 12.6‰ and a δ 15 N value of 15.3‰, reflecting the consumption of marine fish, which, based on medieval written testimonies, were used as fodder in the area during the sampled period 35 . Finally, two donkeys have a δ 13 C value difference of 6.3‰ (− 19.9‰ and − 13.6‰) and a δ 15 N value difference of 2.3‰ (8.0‰ and 10.3‰) that reflect a dependence on C 3 and C 4 plants, respectively, the latter perhaps from coastal environments.
Isotopic results from Siraf. Cats from Siraf have a mean ± SD δ 13 C value of − 12.1 ± 0.9‰ and a mean ± SD δ 15 N value of 12.3 ± 0.5‰, suggesting the consumption of protein from C 4 sources and perhaps some contribution of marine protein. The lesser contribution of marine protein to the diet of these cats is also supported by the results of the mixing model (Supplementary Table S6), which suggest that 34 ± 19% of the protein consumed by the cats was derived from fish and 37 ± 21% from herbivorous mammals. The 20 fish specimens that yielded acceptable isotopic results have a mean ± SD δ 13 C value of − 9.8 ± 4.0‰ and a mean ± SD δ 15 N   Table S3 presents a list of the coastal and pelagic fish from the two sites.

Discussion
Cat diets in Qalhât and Siraf. Due to their peculiar ecological and behavioral features, cats can be both autonomous predators as well as dependent on food provisioning by humans 23,76 . Hunting of wild prey is more significant in rural areas, where anthropogenic food is scarcer 13 . Cats that are independent on food availability by humans and their activities, have been shown to exhibit low δ 13 C and δ 15 N values and narrow value ranges, which reflect a specialized trophic niche that is based on small wild animals 17,23 . Cats from urban contexts, however, are expected to exhibit a wide δ 13 C value range that reflects access to a variety of food sources through humans, as well as high δ 15 N values, especially if marine resources are available 17 . The cats included in the present study come from urban contexts. In Siraf, cat remains were discovered in the commercial heart of the town, the area of the Great Mosque, which was surrounded by shops 36,47 , while in Qalhât, they were found in various buildings across the medieval town 43 . Thus, it is expected that, either by direct feeding and/or scavenging on human food scraps, the Siraf and Qalhât cats consumed foods that they would not be able to access otherwise, for example, meat from large mammals, such as sheep and cattle, as well as fish.
In Qalhât, cats have a 0.4‰ lower mean δ 13 C value, but a 2.8‰ higher mean δ 15 N value than the marine fish, which indicates that marine protein contributed significantly to the diet of the cats from this site. The fact that cats have a similar mean δ 13 C value to the finless porpoise and the small delphinid, but a 1.5-2.0‰ higher mean δ 15 N value, supports this interpretation and further indicates that cats consumed protein of higher trophic level than these two marine mammals, which commonly feed on small fish, crustaceans, cephalopods and other molluscs. Moreover, although cats and red foxes target the same prey groups 77 , the red fox from Qalhât has a 7.0‰ lower δ 15 N value than the mean δ 15 N value of the cats, reflecting the consumption of small prey that was of lesser dietary significance for the domestic cats. Seabirds as well as rats feeding on both fish and seabirds could have also been part of the diet of the Qalhât cats [78][79][80][81] . According to our FRUITS model, rats and birds (including seabirds) may have constituted, respectively, ~ 16% and ~ 21% of the dietary protein consumed by these cats.
Although the mean δ 13 C value of the Siraf cats is only 0.3‰ lower than the mean δ 13 C value of the cats from Qalhât, the 4.8‰ mean δ 15 N value difference between the cats from the two sites, suggests the consumption of lower trophic level foods by the Siraf cats. This mean value difference in nitrogen is statistically significant (p < 0.001). Having a 3.1‰ lower mean δ 13 C value and a 0.6‰ higher mean δ 15 N value compared to the analyzed fish, cats from Siraf were less dependent on marine protein than the cats from Qalhât. This is further supported by the results of the mixing model (Supplementary Table S6), which suggest that ~ 41% of the protein consumed by the cats from Qalhât derived from marine resources, compared to only ~ 34% for the cats from Siraf, with herbivorous mammals comprising their highest dietary contribution (~ 37%). Therefore, the high mean δ 13 C value of the cats from Siraf most likely indicates their dietary dependence on animals who fed on C 4 plants, with a small contribution of protein from marine sources for those with higher δ 15 N values. Different cat diets and local baselines. Although both Siraf and Qalhât are coastal sites (Fig. 1) and were major harbors during the investigated periods 42,47 , cats from the two sites seem to have had different diets. For  www.nature.com/scientificreports/ urban cats, anthropogenic food comprises an important part of their diet 13 . Hence, the different diets observed in the cats from the two sites may be related to the composition of waste resulting from human food preparation and consumption on the one hand and its accessibility and corresponding feeding opportunities offered in the cats' respective home ranges on the other. Although it was not possible to analyze human bone samples from either site, archaeological and historical evidence provide information on the availability of food sources in Siraf and Qalhât during the studied periods. Historical information and archaeobotanical evidence indicate that fruit (especially dates), cereals (including wheat, rice, sorghum and millet) and vegetables (e.g., garlic and eggplant) were either cultivated and/or imported in pre-Islamic and Islamic Oman 72,74,75,82 , including medieval Qalhât 73,83 . The three rat specimens with lower δ 15 N values that were primarily feeding on crops, corroborate the presence of such plants at the site and likely their importance in human diets. Archaeological evidence of plant remains, such as dates 84 , grapes 85 , millet and wheat 86,87 , is also present in prehistoric Iran. Crops, such as wheat and barley, were paid as taxes during the medieval period 88 , when water mills close to Siraf were likely used for grinding cereals 47 . According to the zooarchaeological record, subsistence in Qalhât and Siraf was based on marine fish and domestic animals ( Table 1). Hunting of wild mammals and birds was rarely practiced and occasionally larger marine vertebrates (turtles and delphinoids) were captured, probably as a bycatch of fishing activities. The proportion of the domestic animal bones is higher in Siraf, suggesting that fish contributed less to the human diet in this site compared to Qalhât. Historical sources nevertheless support a high consumption of fish both in Oman 35 as well as in the coast of the Arabian Gulf 34 . In Oman, both small fish, such as sardines and anchovies, as well as larger fish, such as sharks and sailfish, were consumed likely after being sun-dried or salted 35 . Thick layers of fish bones discovered in the domestic building B94, where some of the cat remains analyzed in the present study were also found, may indicate the use of the building for fish processing activities 89 . Such activities, however, may have also taken place on the beach, providing subsistence opportunities to animals, such as seabirds, rats and cats 35 .
In Qalhât, pelagic fishing seems to have been more important than coastal, inshore fishing ( Table 1). The 18 pelagic and four coastal fish from this site have a lower mean δ 13 C value (− 11.3 ± 1.1‰ and − 12.1 ± 1.1‰, respectively) compared to the four pelagic (− 9.6 ± 0.9‰) and 16 coastal (− 8.9 ± 1.0‰) fish from Siraf (Fig. 2,  Supplementary Table S3). In the Arabian Gulf, high temperatures and high evaporation rates lead to hypersaline conditions 90,91 , which result in the underdevelopment of the mangrove tree populations 92,93 . A benthic trophic pathway in microphytobenthos sites, which are 13 C-enriched compared to mangrove sites 94,95 , may, thus, account for the higher δ 13 C values of the fish from Siraf. Moreover, fish from Qalhât, both coastal and pelagic (Fig. 2), have higher δ 15 N values compared to fish from Siraf (Fig. 3), which indicates perhaps a longer trophic chain in the Oman Gulf (although the δ 15 N value differences between fish from the two Gulfs could be also attributed to baseline δ 15 N variations 96 ). The high trophic level of the fish available in Qalhât is seen in the high δ 15 N values of the cats that probably consumed fish, such as longtail tuna and requiem shark, which are the most represented fish categories from the site 37 , and/or seabirds and rats that fed on fish 78,80,81 .
The zooarchaeological evidence from both sites indicates also that among the domestic species, sheep and goats were the most important, with a representation in the skeletal assemblage of > 90% (Table 1). In Qalhât, the wide value ranges (δ 13 C: 1.7‰ and δ 15 N: 2.9‰) for sheep and goats suggest a diet with various amounts of C 4 protein (perhaps partially at coastal areas and salty grounds) as well as potentially a dietary contribution of marine protein (especially for one sheep with a δ 15 N value of > 15.0‰). Similar isotopic signatures were observed in the ovicaprines from the Islamic site of Qalʿat al-Baḥrayn in Bahrain 97 . The practice of using small fish, especially sardines, as fodder has been reported for Oman by late thirteenth and fourteenth century CE sources 34,35 . Although slightly more present in Siraf (3.0%) than in Qalhât (0.6%), cattle were rare, probably due to the animal's size that requires larger quantities of water to be sustained compared to sheep and goats 98,99 . Cattle are also less tolerant to drinking saline water 100,101 . Coastal Iran and Oman have an arid climate, with low annual precipitation, leading to freshwater shortages and increased salinity, while the majority of the freshwater used originates from groundwater resources 102,103 . Of the five cattle from Siraf, three have isotope values that indicate a high dependence on C 4 plants. There is a high diversity of wild C 4 plants in the region [104][105][106] , while archaeobotanical evidence of millet proves that it has been cultivated in the area for centuries before the studied period 86,87 . Although, at first glance, cattle could not have contributed significantly to the diet of the cats given their low overall representation to the faunal assemblage, it was noted that the Siraf cat remains have been collected in the debris deposited near the Great Mosque, more precisely in the commercial heart of the urban center characterized by shops, where butchers likely practiced their craft as well. Cattle butchers in particular not only need large markets with good sales opportunities, but also produce a lot of offal per capita. Therefore, the comparatively large number of cats in the excavation area in question as well as their isotopic signatures could possibly relate to the presence of such a guild. Additionally, considering that the site has been partially excavated 47 and only 10% of the recovered faunal remains has been analyzed 36 , it is likely that large accumulations of cattle bones associated with butchery activities, such as those reported for early Byzantine Sagalassos in Turkey 107 , were not discovered. An alternative source of C 4 protein for the cats from Siraf could have been small prey that fed on C 4 plants. Yet, the two rats analyzed have lower δ 13 C and similar or higher δ 15 N values than the cats, while the consumption of mainly wild prey would likely result in lower δ 15 N values, similarly to the red fox from Qalhât. This brings us back to the previous point that economic activities in the city center opened up opportunities for Siraf cats to get hold of food with a high C 4 content.
The zooarchaeological evidence from Siraf seems to suggest a lesser dependence on marine protein by humans in the area compared to Qalhât. This is further supported by the isotope values of animals such as dogs and chickens, which have previously been considered as proxies for human diets 97,108,109 (however, see also Refs. 110,111 ) and which have mean δ 13 C values indicative of a terrestrial diet. The higher δ 13 C values of the cats compared to these two animals (mean value difference of about 6.0‰) suggests that, although the marine dietary signal in the cats from Siraf is not as clear as for the cats from Qalhât, cats from both sites seem to represent a stronger proxy www.nature.com/scientificreports/ for the marine resources available in the two regions. This has also been suggested for the Islamic site of Qalʿat al-Baḥrayn, where isotopic analysis of both humans and fauna revealed that despite the large numbers of fish bones at the site, humans and chicken (likely consuming human food scraps) have isotope values that indicate a primarily terrestrial diet, while one cat has a higher δ 13 C value that indicates a higher dietary dependence on marine protein 97 . A higher dependence on marine protein for cats, compared to animals that were perhaps mainly feeding on the waste of human food preparation and consumption, likely indicates that these felids were roaming freely, scavenging both on human food scraps as well as on refuse related to on-site processing of fish. The clearer isotopic signal of a marine diet for the cats from Qalhât probably relates to more extended fishing activities in this site, which further included large pelagic species. Finally, cats (and animals in general) are viewed favorably in Islamic culture 112,113 , however, the high mortality of juvenile cats in Qalhât along with the presence of skeletal pathologies (including traumatic lesions) observed in at least two cats 43,45 , may be partially indicative of occasional human violence towards cats. An overall lower human tolerance of cats in this town could have restricted them to the harbor, where large fish were probably gutted prior to further processing. Conversely, the cats that roamed the city center of Siraf may have frequented mainly the immediate surroundings of the market place with its shops, where the processing and sale of fish may have been one activity among many.
Cat diets at seaport sites. A marine dietary signal has also been reported for cats from medieval port towns in Europe. In a recent study, Krajcarz et al. 17 analysed cat remains from various sites, both coastal and inland, in Poland, Germany and Belgium and reported higher δ 13 C and δ 15 N values for the cats from the coastal sites. Krajcarz et al. 17 further reported δ 13 C and δ 15 N differences between cats from port sites located in the Baltic Sea region (Puck, Gdańsk and Kołobrzeg in Poland) and those found in the North Sea region (Bremen in Germany and Nieuwpoort in Belgium), analogous to isotopic value differences reported for fish by Barrett et al. 114 , i.e., both δ 13 C and δ 15 N values being lower for the Baltic Sea, where there is a larger freshwater input. Although cats from Qalhât and Siraf have higher δ 13 C and δ 15 N values than the Polish, German and Belgian cats reported by Krajcarz et al. 17 (Fig. 4, Supplementary Table S4), these differences are most likely related to local isotopic baselines. What remains evident, however, from both studies, is that cats are opportunistic animals that adjust their diets based on the availability of local resources.

Conclusions
By establishing local isotopic baselines, this study generated new evidence on the diet of cats from the medieval harbor sites of Siraf in Iran and Qalhât in Oman. The δ 13 C and δ 15 N results suggest different dietary habits, with the cats from Qalhât being highly dependent on fish and animals feeding on fish, and the cats from Siraf having a mixed marine-terrestrial (C 4 ) diet. This C 4 signal is potentially related to the consumption of cattle meat and offal, however, additional isotopic analyses (i.e., hydrogen stable isotope analysis 115 and compound-specific stable isotope analysis of amino acids 116,117 ) may help to provide a clearer dietary reconstruction in the future.
With an augmented interest in keeping cats as pets 118 and research showing the benefits for mental health in living with companion animals (e.g., Refs. 119,120 ), it becomes increasingly important to learn more about the www.nature.com/scientificreports/ interactions between humans and cats in space and time. By reconstructing the diet of domestic cats from two harbors in the Arabian Gulf and the Gulf of Oman, this study revealed that these felids were most likely roaming freely, scavenging on both the waste of human food consumption as well as refuse related to fishing activities, and, thus, representing an enhanced proxy for the marine dietary protein component of the human diet. The dietary differences between cats from Siraf and Qalhât indicate either differences in the availability of marine resources and/or distinct living conditions, induced by the specific feeding opportunities offered in the anthropogenic space of the two sites. A dietary reconstruction of domestic cats from various sites and periods could shed more light on how humans and cats interacted, thereby creating both unique bonds and mutual dependencies 121,122 that resulted in cats being one of the most popular pets in the world today 118 .

Data availability
All data generated or analyzed during this study are included in this published article (and its Supplementary Information file).